Novel roles of the unfolded protein response in the control of tumor development and aggressiveness

Seminars in Cancer Biology

Volumn 33, Issue , 2015, Pages 67-73

  Dejeans, Nicolas ^a,b   Barroso, Kim ^a,b,c   Fernandez Zapico, Martin E ^c   Samali, Afshin ^d   Chevet, Eric ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c MAYO CLINIC   (United States)

^d NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Cancer; EMT; Endoplasmic reticulum; Stress; Tumor

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; CELECOXIB; CHLOROQUINE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; IMATINIB; INITIATION FACTOR 2ALPHA; PER1 PROTEIN; SCLEROPROTEIN; TRANSCRIPTION FACTOR NRF2; X BOX BINDING PROTEIN 1;

ANGIOGENESIS; AUTOPHAGY; BREAST CARCINOMA; CANCER GROWTH; CANCER INHIBITION; CELL DEATH; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSFORMATION; COLORECTAL CANCER; DIGESTIVE SYSTEM CANCER; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENVIRONMENTAL STRESS; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; GENE EXPRESSION; GLIOBLASTOMA; HEMATOLOGIC MALIGNANCY; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; MALIGNANT TRANSFORMATION; PHENOTYPE; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TRIPLE NEGATIVE BREAST CANCER; UNFOLDED PROTEIN RESPONSE; ANIMAL; APOPTOSIS; CELL MEMBRANE; DISEASE COURSE; DRUG RESISTANCE; GASTROINTESTINAL TUMOR; HOMEOSTASIS; METABOLISM; MOUSE; NEOPLASM; PATHOLOGY;

ANIMALS; APOPTOSIS; CELL MEMBRANE; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; GASTROINTESTINAL NEOPLASMS; HOMEOSTASIS; HUMANS; MICE; NEOPLASMS; PHENOTYPE; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84938203694     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2015.04.007     Document Type: Review

References (89)

1. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
2. Dejeans N., Manie S., Hetz C., Bard F., Hupp T., Agostinis P., et al. Addicted to secrete - novel concepts and targets in cancer therapy. Trends Mol Med 2014, 20:242-250.
3. Garg A., Maes H., van Vliet A.R., Agostinis P. Targeting the hallmarks of cancer with therapy-induced endoplasmic reticulum (ER) stress. Mol Cell Oncol 2015, [in press].
4. Yoshida H., Matsui T., Yamamoto A., Okada T., Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 2001, 107:881-891.
5. Maurel M., Chevet E., Tavernier J., Gerlo S. Getting RIDD of RNA: IRE1 in cell fate regulation. Trends Biochem Sci 2014, 39:245-254.
6. Lee A.H., Iwakoshi N.N., Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 2003, 23:7448-7459.
7. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress National Institute of Environmental Health Sciences. Mol Cell 2003, 11:619-633.
8. Wu J., Rutkowski D.T., Dubois M., Swathirajan J., Saunders T., Wang J., et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell 2007, 13:351-364.
9. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
10. Hetz C., Chevet E., Harding H.P. Targeting the unfolded protein response in disease. Nat Rev Drug Discov 2013, 12:703-719.
11. Rutkowski D.T., Hegde R.S. Regulation of basal cellular physiology by the homeostatic unfolded protein response. J Cell Biol 2010, 189:783-794.
12. Reimold A.M., Iwakoshi N.N., Manis J., Vallabhajosyula P., Szomolanyi-Tsuda E., Gravallese E.M., et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature 2001, 412:300-307.
13. Zhang K., Wong H.N., Song B., Miller C.N., Scheuner D., Kaufman R.J. The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis. J Clin Invest 2005, 115:268-281.
14. Tsang K.Y., Chan D., Bateman J.F., Cheah K.S. In vivo cellular adaptation to ER stress: survival strategies with double-edged consequences. J Cell Sci 2010, 123:2145-2154.
15. Sha H., He Y., Chen H., Wang C., Zenno A., Shi H., et al. The IRE1alpha-XBP1 pathway of the unfolded protein response is required for adipogenesis. Cell Metab 2009, 9:556-564.
16. Ma Y., Hendershot L.M. The role of the unfolded protein response in tumour development: friend or foe?. Nat Rev Cancer 2004, 4:966-977.
17. Delepine M., Nicolino M., Barrett T., Golamaully M., Lathrop G.M., Julier C. EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat Genet 2000, 25:406-409.
18. Harding H.P., Zeng H., Zhang Y., Jungries R., Chung P., Plesken H., et al. Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol Cell 2001, 7:1153-1163.
19. Lin W., Harding H.P., Ron D., Popko B. Endoplasmic reticulum stress modulates the response of myelinating oligodendrocytes to the immune cytokine interferon-gamma. J Cell Biol 2005, 169:603-612.
20. Wang W., Lian N., Li L., Moss H.E., Wang W., Perrien D.S., et al. Atf4 regulates chondrocyte proliferation and differentiation during endochondral ossification by activating Ihh transcription. Development 2009, 136:4143-4153.
21. Zhang P., McGrath B., Li S., Frank A., Zambito F., Reinert J., et al. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 2002, 22:3864-3874.
22. Lin C.Y., Lovén J., Rahl P.B., Paranal R.M., Burge C.B., Bradner J.E., et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 2012, 151:56-67.
23. Nie Z., Hu G., Wei G., Cui K., Yamane A., Resch W., et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 2012, 151:68-79.
24. Torres E.M., Sokolsky T., Tucker C.M., Chan L.Y., Boselli M., Dunham M.J., et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science (New York, NY) 2007, 317:916-924.
25. Tang Y.C., Williams B.R., Siegel J.J., Amon A. Identification of aneuploidy-selective antiproliferation compounds. Cell 2011, 144:499-512.
26. Barna M., Pusic A., Zollo O., Costa M., Kondrashov N., Rego E., et al. Suppression of Myc oncogenic activity by ribosomal protein haploinsufficiency. Nature 2008, 456:971-975.
27. Huber A.L., Lebeau J., Guillaumot P., Petrilli V., Malek M., Chilloux J., et al. p58(IPK)-Mediated attenuation of the proapoptotic PERK-CHOP pathway allows malignant progression upon low glucose. Mol Cell 2013, 49:1049-1059.
28. Bissell M.J., Hines W.C. Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 2011, 17:320-329.
29. Leung C.T., Brugge J.S. Outgrowth of single oncogene-expressing cells from suppressive epithelial environments. Nature 2012, 482:410-413.
30. Mahadevan N.R., Rodvold J., Sepulveda H., Rossi S., Drew A.F., Zanetti M. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc Natl Acad Sci U S A 2011, 108:6561-6566.
31. Mahadevan N.R., Zanetti M. Tumor stress inside out: cell-extrinsic effects of the unfolded protein response in tumor cells modulate the immunological landscape of the tumor microenvironment. J Immunol 2011, 187:4403-4409.
32. Senovilla L., Vitale I., Martins I., Tailler M., Pailleret C., Michaud M., et al. An immunosurveillance mechanism controls cancer cell ploidy. Science (New York, NY) 2012, 337:1678-1684.
33. Luo B., Lee A.S. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 2013, 32:805-818.
34. Heijmans J., van Lidth de Jeude J.F., Koo B.K., Rosekrans S.L., Wielenga M.C., van de Wetering M., et al. ER stress causes rapid loss of intestinal epithelial stemness through activation of the unfolded protein response. Cell Rep 2013, 3:1128-1139.
35. Vermeulen L., Snippert H.J. Stem cell dynamics in homeostasis and cancer of the intestine. Nat Rev Cancer 2014, 14:468-480.
36. Bertolotti A., Wang X., Novoa I., Jungreis R., Schlessinger K., Cho J.H., et al. Increased sensitivity to dextran sodium sulfate colitis in IRE1beta-deficient mice. J Clin Invest 2001, 107:585-593.
37. Tsuru A., Fujimoto N., Takahashi S., Saito M., Nakamura D., Iwano M., et al. Negative feedback by IRE1beta optimizes mucin production in goblet cells. Proc Natl Acad Sci U S A 2013, 110:2864-2869.
38. Kaser A., Lee A.-H., Franke A., Glickman J.N., Zeissig S., Tilg H., et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 2008, 134:743-756.
39. Niederreiter L., Fritz T.M., Adolph T.E., Krismer A.M., Offner F.A., Tschurtschenthaler M., et al. ER stress transcription factor Xbp1 suppresses intestinal tumorigenesis and directs intestinal stem cells. J Exp Med 2013, 210:2041-2056.
40. Adolph T.E., Tomczak M.F., Niederreiter L., Ko H.J., Bock J., Martinez-Naves E., et al. Paneth cells as a site of origin for intestinal inflammation. Nature 2014, 503:272-276.
41. Wu C., Kraft P., Zhai K., Chang J., Wang Z., Li Y., et al. Genome-wide association analyses of esophageal squamous cell carcinoma in Chinese identify multiple susceptibility loci and gene-environment interactions. Nat Genet 2012, 44:1090-1097.
42. Rosekrans S.L., Heijmans J., Buller N.V., Westerlund J., Lee A.S., Muncan V., et al. ER stress induces epithelial differentiation in the mouse oesophagus. Gut 2014.
43. Pohler E., Craig A.L., Cotton J., Lawrie L., Dillon J.F., Ross P., et al. The Barrett's antigen anterior gradient-2 silences the p53 transcriptional response to DNA damage. Mol Cell Proteomics 2004, 3:534-547.
44. Carrasco D.R., Sukhdeo K., Protopopova M., Sinha R., Enos M., Carrasco D.E., et al. The differentiation and stress response factor XBP-1 drives multiple myeloma pathogenesis. Cancer Cell 2007, 11:349-360.
45. Kharabi Masouleh B., Geng H., Hurtz C., Chan L.N., Logan A.C., Chang M.S., et al. Mechanistic rationale for targeting the unfolded protein response in pre-B acute lymphoblastic leukemia. Proc Natl Acad Sci U S A 2014, 111:E2219-E2228.
46. Rouault-Pierre K., Lopez-Onieva L., Foster K., Anjos-Afonso F., Lamrissi-Garcia I., Serrano-Sanchez M., et al. HIF-2alpha protects human hematopoietic stem/progenitors and acute myeloid leukemic cells from apoptosis induced by endoplasmic reticulum stress. Cell Stem Cell 2013, 13:549-563.
47. Pattacini L., Mancini M., Mazzacurati L., Brusa G., Benvenuti M., Martinelli G., et al. Endoplasmic reticulum stress initiates apoptotic death induced by STI571 inhibition of p210 bcr-abl tyrosine kinase. Leuk Res 2004, 28:191-202.
48. Higa A., Taouji S., Lhomond S., Jensen D., Fernandez-Zapico M.E., Simpson J.C., et al. Endoplasmic reticulum stress-activated transcription factor ATF6alpha requires the disulfide isomerase PDIA5 to modulate chemoresistance. Mol Cell Biol 2014, 34:1839-1849.
49. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
50. Nieto M.A., Cano A. The epithelial-mesenchymal transition under control: global programs to regulate epithelial plasticity. Semin Cancer Biol 2012, 22:361-368.
51. Baum B., Settleman J., Quinlan M.P. Transitions between epithelial and mesenchymal states in development and disease. Semin Cell Dev Biol 2008, 19:294-308.
52. Schmalhofer O., Brabletz S., Brabletz T. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 2009, 28:151-166.
53. Clarke H.J., Chambers J.E., Liniker E., Marciniak S.J. Endoplasmic reticulum stress in malignancy. Cancer Cell 2014, 25:563-573.
54. Ulianich L., Garbi C., Treglia A.S., Punzi D., Miele C., Raciti G.A., et al. ER stress is associated with dedifferentiation and an epithelial-to-mesenchymal transition-like phenotype in PC Cl3 thyroid cells. J Cell Sci 2008, 121:477-486.
55. Feng Y.X., Sokol E.S., Del Vecchio C.A., Sanduja S., Claessen J.H., Proia T.A., et al. Epithelial-to-mesenchymal transition activates PERK-eIF2alpha and sensitizes cells to endoplasmic reticulum stress. Cancer Discov 2014, 4:702-715.
56. Del Vecchio C.A., Feng Y., Sokol E.S., Tillman E.J., Sanduja S., Reinhardt F., et al. De-differentiation confers multidrug resistance via noncanonical PERK-Nrf2 signaling. PLOS Biol 2014, 12:e1001945.
57. Tanjore H., Cheng D.S., Degryse A.L., Zoz D.F., Abdolrasulnia R., Lawson W.E., et al. Alveolar epithelial cells undergo epithelial-to-mesenchymal transition in response to endoplasmic reticulum stress. J Biol Chem 2011, 286:30972-30980.
58. Carlisle R.E., Heffernan A., Brimble E., Liu L., Jerome D., Collins C.A., et al. TDAG51 mediates epithelial-to-mesenchymal transition in human proximal tubular epithelium. Am J Physiol Renal Physiol 2012, 303:F467-F481.
59. Sheshadri N., Catanzaro J.M., Bott A., Sun Y., Ullman E., Chen E., et al. SCCA1/SerpinB3 promotes oncogenesis and epithelial-mesenchymal transition via the unfolded protein response and IL-6 signaling. Cancer Res 2014.
60. Gao S.P., Mark K.G., Leslie K., Pao W., Motoi N., Gerald W.L., et al. Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest 2007, 117:3846-3856.
61. Sansone P., Storci G., Tavolari S., Guarnieri T., Giovannini C., Taffurelli M., et al. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 2007, 117:3988-4002.
62. Kirk S.J., Cliff J.M., Thomas J.A., Ward T.H. Biogenesis of secretory organelles during B cell differentiation. J Leukoc Biol 2009, 87:245-255.
63. Fox R.M., Hanlon C.D., Andrew D.J. The CrebA/Creb3-like transcription factors are major and direct regulators of secretory capacity. J Cell Biol 2010, 191:479-492.
64. Zeindl-Eberhart E., Brandl L., Liebmann S., Ormanns S., Scheel S.K., Brabletz T., et al. Epithelial-mesenchymal transition induces endoplasmic-reticulum-stress response in human colorectal tumor cells. PLOS ONE 2014, 9:e87386.
65. Spaderna S., Schmalhofer O., Wahlbuhl M., Dimmler A., Bauer K., Sultan A., et al. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res 2008, 68:537-544.
66. Vandewalle C., Van Roy F., Berx G. The role of the ZEB family of transcription factors in development and disease. Cell Mol Life Sci 2009, 66:773-787.
67. Alam J., Stewart D., Touchard C., Boinapally S., Choi A.M., Cook J.L. Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 1999, 274:26071-26078.
68. Alam J., Wicks C., Stewart D., Gong P., Touchard C., Otterbein S., et al. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells, role of p38 kinase and Nrf2 transcription factor. J Biol Chem 2000, 275:27694-27702.
69. Maines M.D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J 1988, 2:2557-2568.
70. Lee J.Y., Chang J.W., Yang W.S., Kim S.B., Park S.K., Park J.S., et al. Albumin-induced epithelial-mesenchymal transition and ER stress are regulated through a common ROS-c-Src kinase-mTOR pathway: effect of imatinib mesylate. Am J Physiol Renal Physiol 2011, 300:F467-F481.
71. Curran M.P., McKeage K. Bortezomib: a review of its use in patients with multiple myeloma. Drugs 2009, 69:859-888.
72. Hong M., Kim H., Kim I. Ribosomal protein L19 overexpression activates the unfolded protein response and sensitizes MCF7 breast cancer cells to endoplasmic reticulum stress-induced cell death. Biochem Biophys Res Commun 2014, 450:673-678.
73. Adamson C., Kanu O.O., Mehta A.I., Di C., Lin N., Mattox A.K., et al. Glioblastoma multiforme: a review of where we have been and where we are going. Expert Opin Investig Drugs 2009, 18:1061-1083.
74. Westphal M., Lamszus K. The neurobiology of gliomas: from cell biology to the development of therapeutic approaches. Nat Rev Neurosci 2011, 12:495-508.
75. Zhong J., Paul A., Kellie S.J., O'Neill G.M. Mesenchymal migration as a therapeutic target in glioblastoma. J Oncol 2010, 2010:430142.
76. Phillips H.S., Kharbanda S., Chen R., Forrest W.F., Soriano R.H., Wu T.D., et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 2006, 9:157-173.
77. Carro M.S., Lim W.K., Alvarez M.J., Bollo R.J., Zhao X., Snyder E.Y., et al. The transcriptional network for mesenchymal transformation of brain tumours. Nature 2010, 463:318-325.
78. Greenman C., Stephens P., Smith R., Dalgliesh G.L., Hunter C., Bignell G., et al. Patterns of somatic mutation in human cancer genomes. Nature 2007, 446:153-158.
79. Parsons D.W., Jones S., Zhang X., Lin J.C.-H., Leary R.J., Angenendt P., et al. An integrated genomic analysis of human glioblastoma multiforme. Science (New York, NY) 2008, 321:1807-1812.
80. Auf G., Jabouille A., Guerit S., Pineau R., Delugin M., Bouchecareilh M., et al. Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma. Proc Natl Acad Sci U S A 2010, 107:15553-15558.
81. Drogat B., Auguste P., Nguyen D.T., Bouchecareilh M., Pineau R., Nalbantoglu J., et al. IRE1 signaling is essential for ischemia-induced vascular endothelial growth factor-A expression and contributes to angiogenesis and tumor growth in vivo. Cancer Res 2007, 67:6700-6707.
82. Pluquet O., Dejeans N., Bouchecareilh M., Lhomond S., Pineau R., Higa A., et al. Posttranscriptional regulation of PER1 underlies the oncogenic function of IREalpha. Cancer Res 2013, 73:4732-4743.
83. Dejeans N., Pluquet O., Lhomond S., Grise F., Bouchecareilh M., Juin A., et al. Autocrine control of glioma cells adhesion and migration through IRE1alpha-mediated cleavage of SPARC mRNA. J Cell Sci 2012, 125:4278-4287.
84. Foulkes W.D., Smith I.E., Reis-Filho J.S. Triple-negative breast cancer. N Engl J Med 2010, 363:1938-1948.
85. Lehmann B.D., Bauer J.A., Chen X., Sanders M.E., Chakravarthy A.B., Shyr Y., et al. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011, 121:2750-2767.
86. Chen X., Iliopoulos D., Zhang Q., Tang Q., Greenblatt M.B., Hatziapostolou M., et al. XBP1 promotes triple-negative breast cancer by controlling the HIF1alpha pathway. Nature 2014, 508:103-107.
87. Lu Y., Liang F.X., Wang X. A synthetic biology approach identifies the mammalian UPR RNA ligase RtcB. Mol Cell 2014, 55:758-770.
88. Li H., Chen X., Gao Y., Wu J., Zeng F., Song F. XBP1 induces snail expression to promote epithelial-to-mesenchymal transition and invasion of breast cancer cells. Cell Signal 2014.
89. Thomas S., Sharma N., Golden E.B., Cho H., Agarwal P., Gaffney K.J., et al. Preferential killing of triple-negative breast cancer cells in vitro and in vivo when pharmacological aggravators of endoplasmic reticulum stress are combined with autophagy inhibitors. Cancer Lett 2012, 325:63-71.